Gut Microbes
ISSN: 1949-0976 (Print) 1949-0984 (Online) Journal homepage: http://www.tandfonline.com/loi/kgmi20
Bifidobacterium animalis subspecies lactis modulates the local immune response and glucose uptake in the small intestine of juvenile pigs infected with the parasitic nematode Ascaris suum Gloria Solano-Aguilar, Terez Shea-Donohue, Kathleen B. Madden, Alejandro Quinoñes, Ethiopia Beshah, Sukla Lakshman, Yue Xie, Harry Dawson & Joseph F. Urban To cite this article: Gloria Solano-Aguilar, Terez Shea-Donohue, Kathleen B. Madden, Alejandro Quinoñes, Ethiopia Beshah, Sukla Lakshman, Yue Xie, Harry Dawson & Joseph F. Urban (2018): Bifidobacterium�animalis�subspecies�lactis modulates the local immune response and glucose uptake in the small intestine of juvenile pigs infected with the parasitic nematode Ascaris�suum, Gut Microbes, DOI: 10.1080/19490976.2018.1460014 To link to this article: https://doi.org/10.1080/19490976.2018.1460014
© 2018 The Author(s). Published by Taylor & Francis. Published online: 19 Jul 2018.
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GUT MICROBES https://doi.org/10.1080/19490976.2018.1460014
RESEARCH PAPER
Bifidobacterium animalis subspecies lactis modulates the local immune response and glucose uptake in the small intestine of juvenile pigs infected with the parasitic nematode Ascaris suum ~esd, Ethiopia Beshaha, Gloria Solano-Aguilara, Terez Shea-Donohueb, Kathleen B. Maddenc, Alejandro Quinon a e a a Sukla Lakshman , Yue Xie , Harry Dawson , and Joseph F. Urban a United States Department of Agriculture, Agricultural Research Service, Beltsville Human Nutrition Research Center, Diet Genomics and Immunology Laboratory, Beltsville, MD; bDepartment of Radiation Oncology, University of Maryland School of Medicine, Baltimore, MD; c Department of Pediatrics, Uniformed Services University of the Health Sciences, Bethesda, MD; dUniversity of California, Riverside Campus, CA; e Department of Parasitology, Sichuan Agricultural University, College of Veterinary Medicine, Sichuan, China
ABSTRACT
ARTICLE HISTORY
An evaluation of a localized intestinal allergic type-2 response concomitant with consumption of probiotic bacteria is not well documented. This study investigated the effect of feeding probiotic Bifidobacterium animalis subspecies lactis (Bb12) or a placebo in weaned pigs that were also inoculated with Ascaris suum (A. suum) eggs to induce a strong Th2-dependent allergic type 2 immune response. Sections of jejunal mucosa were mounted in Ussing chambers to determine changes in permeability and glucose absorption, intestine and liver samples were collected for analysis of type-2 related gene expression, jejunum examined histologically, and sera and intestinal fluid were assayed for parasite antigen specific antibody. The prototypical parasite-induced secretory response to histamine and reduced absorption of glucose in the jejunum were attenuated by feeding Bb12 without a change in mucosal resistance. Parasite antigen-specific IgA response in the serum and IgG1 and IgG2 response in the ileal fluid were significantly increased in A. suuminfected pigs treated with Bb12 compared to infected pigs given the placebo. Ascaris suum-induced eosinophilia in the small intestinal mucosa was inhibited by Bb12 treatment without affecting the normal expulsion of A. suum 4th stage larvae (L4) or the morphometry of the intestine. Expression of genes associated with Th1/Th2 cells, Treg cells, mast cells, and physiological function in the intestine were modulated in A. suum infected-pigs treated with Bb12. These results suggested that Bb12 can alter local immune responses and improve intestinal function during a nematode infection by reducing components of a strong allergenic type-2 response in the pig without compromising normal parasite expulsion.
Received 2 October 2017 Revised 18 March 2018 Accepted 26 March 2018
Introduction Two major functions of the intestinal epithelium are to provide a selective barrier to luminal contents and to transport water, nutrients, and electrolytes.1-3 The intestinal epithelium is also the interface between luminal contents and the mucosal immune system. It functions not only to reduce responses to food antigens and commensal bacteria, but to activate host defenses against pathogens.4 Alterations in epithelial barrier function, therefore, can play a significant role in regulating gastrointestinal disease.5 Infection with gastrointestinal parasites affects the physiological and immunological responses of the host. Helminth infection induces a hyper-contractility of CONTACT Gloria Solano-Aguilar USA.
[email protected]
KEYWORDS
Probiotic; Th2 cytokines; nematode infection; immune modulation; intestinal function; eosinophil infiltration
intestinal smooth muscle, inhibition of intestinal glucose absorption, and changes in intestinal secretion that are IL-4 receptor-dependent and STAT6-inducible.6 There is growing interest in the use of probiotics to ameliorate the negative effects of infection and allergic disease.7 Probiotics have been used to treat a variety of gastrointestinal (GI) ailments including inflammatory bowel disease (IBD), irritable bowel syndrome, viral enteritis, and antibiotic-associated diarrhea.8-11 Although little is known definitively about their mechanism of action, probiotics seem to have protective and anti-inflammatory effects on the intestinal mucosa. Proposed mechanisms include the production of ammonia, hydrogen peroxide, and bacteriocins that inhibit the growth of pathogenic bacteria, 10300 Baltimore Avenue, BARC-East. Bldg 307C, Room 225, Beltsville, MD 20705,
© 2018 the author(s). published by taylor & Francis this is an open access article distributed under the terms of the Creative Commons attribution- non Commercial-no Derivatives License (http://creativecommons.org/licenses/bync-nd/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way.
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G. SOLANO-AGUILAR ET AL.
competition for bacterial adhesion sites on intestinal epithelia, alterations of composition and function of the gut microbiome, and an adjuvant-type stimulation of the immune system against pathogenic organisms.12-16 In the present study, we investigated the effect of Bifidobacterium animalis subspecies lactis (strain Bb12), a humanderived probiotic used extensively in dairy products,17,18 on immune activation and intestinal function of young pigs exposed to migrating A. suum larvae.19 Our results showed that Bb12 modulated the liver and intestinal immune response and intestinal physiology without compromising the normal expulsion of the worms. The parasite-induced reduction in intestinal glucose absorption was ameliorated, the tissue eosinophilic response was reduced, and serum and intestinal antibody responses to the worm were enhanced by feeding Bb12.
Results Quantitative detection of Bifidobacterium animalis subspecies lactis (Bb12) in the intestine
Bb12-treated pigs born to Bb12-treated sows (T/T) had significantly higher copies per gram (cpg) of the Bifidobacterium animalis subspecies lactis tuf gene20 in proximal colon contents of Ascaris suum (A. suum)infected T/T (1.8 § 0.9 £ 105 cpg) compared to non-
infected control placebo-treated pigs born to placebotreated sows (C/C) (0.07 § 0.07 £ 104 cpg; p < 0.05) or A. suum-infected C/C (0.006 § 0.004 £ 104 cpg; p
